Unveiling a new oceanic anoxic event at the Norian/Rhaetian boundary (Late Triassic)

The latest Triassic was characterised by protracted biotic extinctions concluding in the End-Triassic Extinction (~ 200 Ma) and a global carbon cycle perturbation. The onset of declining diversity is closely related to reducing conditions that spread globally from upper Sevatian (uppermost Norian) to across the Norian-Rhaetian boundary, likely triggered by unusually high volcanic activity. We correlate significant organic carbon cycle perturbations to an increase of CO2 in the ocean–atmosphere system, likely outgassed by the Angayucham igneous province, the onset of which is indicated by the initiation of a rapid decline in 87Sr/86Sr and 188Os/187Os seawater values. A possible causal mechanism involves elevated CO2 levels causing global warming and accelerating chemical weathering, which increased nutrient discharge to the oceans and greatly increased biological productivity. Higher export production and oxidation of organic matter led to a global O2 decrease in marine water across the Norian/Rhaetian boundary (NRB). Biotic consequences of dysoxia/anoxia include worldwide extinctions in some fossil groups, such as bivalves, ammonoids, conodonts, radiolarians.

dark to black shales, indicating that the oceanic oxygen depletion events are diachronous across sedimentary basins 1 .Furthermore, OAEs are generally related to sea water warming indicated by low δ 18 O values, which is however commonly interrupted by cooling phases likely caused by the increase of organic matter burial and pCO 2 decrease 1,5 .
Phanerozoic OAEs are defined by intervals of widespread oxygen depletion in the ocean, recognized by sedimentological and/or geochemical records, yet they are significantly dissimilar from each other 5 .Jurassic and Cretaceous OAEs are particularly well-studied, such as the early Toarcian (Posidonienschiefer event, T-OAE, ~ 183 Ma), early Aptian (Selli event, OAE 1a, ~ 120 Ma), early Albian (Paquier event, OAE 1b, ~ 111 Ma) and Cenomanian-Turonian (Bonarelli event, OAE 2, ~ 94 Ma) events 1,8 .Potential forcing mechanisms for OAEs include massive releases of methane (CH 4 ) or volcanogenic carbon dioxide (CO 2 ) outgassing into the atmosphere during the emplacement of Large Igneous Provinces (LIPs) as continental flood basalts or oceanic plateaus 1,9 .For example, OAE 1a correlates to the Ontong Java Plateau, OAE 2 is associated with the Caribbean-Colombian Plateau 1 and the early Toarcian OAE is linked to the Karoo-Ferrar subaerial flood basalt extrusions 10 .Similar scenarios occurred during the late Sevatian (late Norian, Late Triassic) and across the Norian-Rhaetian boundary (NRB), during which significant biotic extinctions of important terrestrial and marine taxa occurred 11 .Notably, cosmopolitan bivalves (e.g., monotids, halobiids) are one of the major fossil groups that suffered a global and severe extinction, starting from the Sevatian to the lowermost Rhaetian [11][12][13] , while ammonoids suffered the largest decline among invertebrates, with a reduction in genera by more than an order of magnitude 14,15 .Other faunal extinctions and diversity loss also are documented for radiolarians and conodonts [16][17][18] , marine vertebrates (e.g., actinopterygian fishes) and reptiles (particularly among ichthyosaurs) 19 .In addition, reef communities declined significantly during the Late Triassic 20 .This interval of strong faunal extinctions at the NRB is associated with large carbon isotope excursions recorded on land 21,22 and in marine environments 11 , which are linked to oscillations of biological pump efficiency and/or ocean stratification 11 .
We investigated and compared redox conditions recorded in several NRB sections deposited in different sedimentary environments (from shallow to deep water) on opposite sides of Pangea, spanning both hemispheres and across latitudes (Fig. 1).The Pignola-Abriola and Sasso di Castalda sections were deposited in the deep pelagic Lagonegro Basin (Italy), which was part of the western Tethys 23,24 .The Lagonegro Basin records the change from carbonate to biosiliceous sedimentation below the carbonate compensation depth (CCD) across the NRB [25][26][27] .Both these sections were previously investigated for bio-and chemostratigraphy 11,[23][24][25][27][28][29][30][31][32][33][34] , while magnetostratigraphy was performed only in Pignola-Abriola section 35 . The suthern Tethys Wombat Basin (NW Australia) was a neritic continental shelf environment located in the southern Tethys on the margin of Pangea, and was recently studied for biostratigraphy 36 and chemostratigraphy 11 .The Kiritehere section (New Zealand) was deposited from mid-shelf to deeper water basin on the southernmost margin of Gondwana, close to the South Pole, and it has been recently investigated for organic carbon 37 .The Holberg section (British Columbia, Canada) is illustrated here for the first time and it represents a shallow to moderate depth depositional environment off an oceanic plateau in eastern Panthalassa, and it has been studied for organic carbon stable isotopes (δ 13 C org ) and chemostratigraphy (this study; Supplementary material).The Katsuyama section (Japan) was deposited below the CCD in the north Equatorial belt of the Panthalassa Ocean has been studied for bio-and chemostratigraphy and δ 13 C org (this study; Supplementary material). Al these sections spanned the uppermost Sevatian to lower Rhaetian, which is usually characterized by laminated layers and dark to black shales, except for the Katsuyama section that consists of red and dark red shales and cherts( 11 and Supplementary material).Notably, the Kiritehere section mostly consists of dark volcanoclastic rocks without any particularly darker portions of the succession.The NRB is identified with the first occurrence of the conodont Misikella posthernsteini or (when necessary) is approximated by the negative δ 13 C org peak just below the base of the Rhaetian 11,24 .The Wombat and Holberg sections and the Calcari con Selce Formation in the Pignola-Abriola and Sasso di Castalda sections are cherty limestones.
Higher concentrations of elements that indicate suboxic to anoxic environments (Cr, V, U, and Mo) were observed in the NRB of the Tethys and eastern Panthalassa oceans (Fig. 1).A slight enrichment of Cr in the Wombat section suggests that at least suboxic conditions existed in the southeastern Tethys Ocean during the NRB interval.Across the NRB, a significant increase in V EF is recorded in sediments deposited in intermediate to deep water environments, represented by the Holberg, Pignola-Abriola and Sasso di Castalda sections (Fig. 1).Vanadium reduction occurs under lower oxygen concentrations 45 .In oxic seawater, V is present as soluble V(V) in the quasi-conservative form of vanadate oxyanions (HVO 4 2-and H 2 VO 4 2-).When conditions change from suboxic to weakly anoxic, V(V) converts to V(IV) and forms the vanadyl ion (VO 2+ ), related hydroxyl species (VO(OH) 3-), and insoluble hydroxides (VO(OH) 2 ) 48,49 .The highest concentration of V is recorded in the NRB of the Pignola-Abriola section, where V EF values are relatively constant and close to the value of 1 in the Sevatian and abruptly increase across the NRB (Fig. 1).Similar V enrichments are found in the NRB of the Holberg and Sasso di Castalda sections.In the Wombat section, V increases across the NRB, indicating that the shallow marine environment in the southeastern Tethys has changed to a suboxic-anoxic environment (Fig. 1).
On the other hand, the lack of V and U enrichments in the shallow marine sections of Kiritehere apparently does not indicate that these shallow depositional environments might have been oxygen-poor too.However, the www.nature.com/scientificreports/Kiritehere section recorded the global extinction of pelagic and benthonic bivalves that belonged to the monitid group, so other mechanisms related to the spread of oxygen-deficient waters might be thus indicated (e.g., ocean acidification, competition, food shortage, eutrophication).In addition, no stratigraphic changes in concentrations of redox-sensitive elements were observed in the deep-sea pelagic deposits of Panthalassa, represented by the Katsuyama section.This suggests that the development of oxygen-poor conditions may not have extended to the deep seafloor of the mid-Panthalassic Ocean (Fig. 1).Another common redox proxy for reducing conditions is the Mo EF /U EF ratio, which shows enrichment trends similar to those observed for V EF in both the Pignola-Abriola and Holberg sections (Fig. 1).Covariations of Mo and U enrichment patterns (Fig. 2) and increased Mo EF /U EF ratios suggest the development of anoxic bottom water and scavenging of Mo by a Fe-Mn (oxyhydr)oxide particulate shuttle during the upper Sevatian to Rhaetian 38,49 .The occurrence of the particulate shuttle requires an oxic-anoxic redox boundary in the water column and rapid water replacement to maintain the predicted Fe-Mn redox behavior 38,50 .Thus, the Mo EF /U EF increase in the particulate shuttle field in the Holberg and Pignola-Abriola sections may indicate the development of intermediate-depth O 2 minima with redox boundaries on both sides of Pangea.However, Mo enrichment due to Mn-and Fe-particulate shuttles was less significant compared to modern sites with anoxic oxygen minimum zones (OMZs) 50 .Consequently, V enrichment and U EF and Mo EF trends suggest that anoxic conditions occurred in mid-to deep-water environments over a large area around Pangaea (Fig. 1).
Mo is a conservative hexavalent oxyanion (MoO 4

2--
) in oxygenated water.The largest sink of Mo in the modern ocean (50%) is adsorption to manganese oxides, which preferentially retains light isotopes.This also occurs in MnO 2 formed on land.Reporting Mo isotope compositions and correcting published data sets to the NIST 3134 reference solution (δ 98 Mo = (( 98 Mo/ 95 Mo) sample /( 98 Mo/ 95 Mo) 3134 -1) × 1000) 51 , river water δ 98 Mo averages + 0.54‰ 52 and seawater + 2.09‰ ± 0.10 51 , higher than the average continental crust based on molybdenite (0.04‰ ± 1.04) 53 or silicate rocks (+ 0.15‰) 54 .As the size of the marine Mn oxide sink of Mo changes over time, depending on the extent of anoxic basins, the δ 98 Mo composition of seawater is expected to also change over time.For example, prior to OAE-2 at 94 Ma, seawater δ 98 Mo was lower (+ 1.65‰) 55 .In conditions where free dissolved sulfide exists at concentrations exceeding 10 mM, Mo is quantitatively removed, and underlying sediments can preserve the isotopic composition of Mo in seawater.Today, euxinic basins are restricted to isolated systems like the Black Sea and fjords where exchange with the open ocean is poor, but in the past they may have been more common.In anoxic but non-euxinic basins, the isotope composition of sedimentary Mo depends on the presence or absence of Mn-oxides and bottom water oxygen.If porewater sulfide is sufficiently close to the sediment-water interface, while bottom water may not be euxinic, seawater Mo can diffuse into the sediment to give them a similar δ 98 Mo to seawater, but the Mo concentration will be lower than in truly euxinic basins 57 .With slightly higher O 2 in bottom water, but with anoxic pore water, Mn-oxides with low δ 98 Mo that formed within seawater can dissolve in the anoxic sediments, releasing their Mo with low δ 98 Mo.This Mo can diffuse up towards the seawater-sediment interface, or down where it can be trapped permanently in deeper, sulfidic sediments.Today, sediment δ 98 Mo can range from ~ -1‰ in fully oxic systems to + 2.0‰ in euxinic systems, with intermediate values corresponding to redox state and the presence of sulfide.While modern ooids have a composition close to the seawater they precipitate from, use of skeletal carbonates (δ 98 Mo carb ) as a proxy of seawater can be affected by non-equilibrium (biological) fractionation.Furthermore, δ 98 Mo of impure carbonates will also reflect contributions from detritus and Fe-Mn oxides, which is much lower than the seawater value.
Samples analysed for Mo isotopes were either carbonate-absent (CaO < 1%) or carbonate-bearing.The Mo in carbonate-absent sediments is derived from detritus or authigenic phases, namely Fe-Mn hydroxide and sulfides, while he carbonate-bearing samples also contain significant amounts of potentially isotopically distinct carbonate.Analyses were made on bulk samples, but to address the isotope composition of seawater derived phases, correction for detrital material is made.This is done by assuming all Ti is detrital, and using the upper continental crust (UCC) Mo/Ti composition to determine the amount of detritus-bound Mo.The isotope composition of the UCC is assumed to represent the detrital material, and for this we use UCC Mo concentrations and isotope composition of 1.1 ppm and + 0.1‰ 58,59 to subtract the detrital contribution to the whole rock data by isotope mass balance, leaving a δ 98 Mo value for authigenic (Fe-Mn hydroxide or sulfide) plus carbonate phases.The highest δ 98 Mo in carbonate will be close to seawater, and our highest δ 98 Mo carb of + 1.65 is similar to that of Cretaceous seawater suggesting that Late Triassic seawater was somewhat similar 55 .In the www.nature.com/scientificreports/Pignola-Abriola section, the δ 98 Mo in carbonate-absent samples increases from -3.5‰ at 30 m to just 0.1‰ at 42.9 m, while the δ 98 Mo in carbonate-bearing samples are more variable (-2.7‰ to + 1.7‰) (Fig. 3).
In an oxic water column, Fe-Mn hydroxides are 3‰ lower in δ 98 Mo than seawater 56 , but the lowest values of δ 98 Mo we measure are more than 3‰ lower than our estimate of seawater at the time of formation.To increase this difference beyond 3‰, dissolution of Fe-Mn hydroxides (bearing low δ 98 Mo signatures) followed by their re-oxidation is indicated, suggesting that the oxygen content of water close to the seawater sediment interface fluctuated in response to physical restriction, which is unlikely given the paleo-reconstruction of the Pignola-Abriola area, or to changes in the delivery of organic matter, supported by the correspondence between the lowest δ 98 Mo and highest TOC%.The increase in δ 98 Mo auth from values consistent with a mostly, albeit variable, oxic water column to values consistent with anoxic to euxinic sediments underlying an expanding area of high productivity with a persistent oxygen minimum zone 61 .The increase in δ 98 Mo auth towards that of contemporaneous seawater indicated by the highest δ 98 Mo carb as Mo EF /U EF also increases supports the concept of intensification of an OMZ driven by increasing productivity, and the progression of a porewater sulfide front towards the sediment-seawater interface.

Possible cause(s)
These environmental perturbations can be explained by various mechanisms, any of which may create a global record, such as dissociation of clathrate hydrate and/or enhanced magmatic activity and outgassing 1,62,63 .Likely, a large volume of 13 C-depleted CO 2 entered the ocean-atmosphere system prior to the NRB, possibly as a product of volcanic outgassing by the emplacement of the Angayucham LIP 11,21,24,32,64 .This hypothesis is supported by the comparison of C-isotope records from marine 11 and terrestrial settings 21,22 with the seawater Sr-isotope 65 and Os-isotope curves [66][67][68] .The 87 Sr/ 86 Sr and 187 Os ⁄ 188 Os values started to decline in the upper Norian, indicating a relative increase in the supply of mantle-derived unradiogenic Sr and Os from marine hydrothermal or other mafic igneous sources.Furthermore, the mechanism invoked to explain the spread of reducing conditions also implies significant input of CO 2 into the ocean-atmosphere system that would enhance chemical weathering via acceleration of the hydrological cycle during radiative-forced warming and cause increased nutrient discharge (e.g., nitrates and phosphates) to the global ocean 1,69,70 .The coincidence of these three concatenated steps has been clearly documented worldwide.Our weathering proxy data (Chemical Index of Alteration-CIA, Rb EF , and K EF values) have revealed that chemical weathering intensified during the development of anoxic conditions (Figs. 3, 4).
Values of the CIA from the shale samples 71 indicate the extent of decomposition of feldspar minerals, which are the most abundant mineral group in the UCC.Because of the high carbonate content of the study section, we used a modified form of the CIA equation by 33 as: CIA values are relatively constant below the FO level of M. posthernsteini s.l.sensu 34 , and then rapidly increase in the S3 interval (sensu 32 , Fig. 3).These stratigraphic variations in CIA values indicate intensified chemical weathering on continents during the S3 interval, implying that the climate changed to relatively warm and humid conditions.K and Rb were released from primary minerals, possibly micas and feldspars in felsic rocks, during continental chemical weathering..δ 98 Mo auth for carbonate-absent is of Fe-Mn hydroxides and for carbonate-bearing is Fe-Mn hydroxides plus carbonate.Strontium curve modified after 64 .A description of the taxonomic range of conodonts is as follows: 1. Mockina bidentata; 2. Parvigondolella andrusovi; 3. Misikella hernsteini; 4. Mi. hernsteini/ posthernsteini; 5. Mi. posthernsteini; 6. Mi. ultima.
In theory, enhanced chemical weathering via acceleration of the hydrological cycle would cause increased nutrient discharge to the global ocean, with a consequent increase in biological productivity 1,70,72 .Barium is commonly used as a tracer of paleo-productivity [73][74][75][76] , because barite precipitation occurs in decaying particulate organic matter while it sinks to the seafloor 74,77,78 , which is supported by enhanced Ba EF values below highproductivity areas 79 .Our data show that Ba EF increased in the NRB, except in the Panthalassic Katsuyama section, deposited below the CCD (Fig. 1).Hence, our geochemical proxies show an apparent link between the volcanic event and oceanic anoxia via increased chemical weathering and paleo-productivity during the S3 interval.
High CIA continues after the boundary, indicating the persistence on land of the conditions that triggered the OAE even as the ocean began to recover, first exhibited by Mo EF /U EF 50 .δ 98 Mo auth also begins to record increasing oxic conditions well after the boundary, showing the control that Mn has on δ 98 Mo.The prolonged chemical weathering could be the result of a million-year timescale required for silicate weathering to consume the massive amounts of CO 2 emitted during volcanism.Long-term increases in CIA similar to the NRB have also been reported from the early Late Triassic Carnian Pluvial Episode (CPE; 232-234 Ma) and from the Triassic-Jurassic boundary 80,81 .In the case of the Triassic-Jurassic boundary, it is estimated that 1-2 myr were necessary for chemical weathering 80 to consume the large amount of CO 2 released by 600 kyr of volcanic activity 82 .CO 2 emissions from voluminous, pulsed volcanic activity across the NRB may have thus caused prolonged continental weathering in the Rhaetian.
In summary, our data document a previously unknown OAE of global extent, similar in nature to other OAEs.The OAE that spanned the NRB extended across the Panthalassa Ocean to both sides of the Pangea supercontinent and it is recorded in both the Northern and Southern Hemispheres, at different latitudes.As is the case for most OAEs, we propose that this Norian-Rhaetian oceanic oxygen depletion event resulted from largevolume emissions of volcanogenic greenhouse gases that accelerated the hydrological cycle, thereby increasing weathering rates and increasing nutrient delivery to the oceans.The increased nutrient supply enhanced primary productivity and export of organic carbon, resulting in oxygen depletion and expansion of the OMZ, which in turn increased the burial efficiency of organic carbon in sediments.Fossil extinctions and reducing conditions were documented in basins around the world (Italy, Canada, NW Australia, New Zealand), leaving an unmistakable record of the NRB OAE.The onset of the stepwise Late Triassic extinctions coincided with the NRB OAE, indicating that the combined climate and environmental changes impacted biota at this time.The trigger of this event is attributed to a volcanic event pre-dating the NRB or an alternative source of volcanogenic gas emissions, likely from the Angayucham LIP.

Figure 1 .
Figure 1.δ13 C org , Ba, and redox-sensitive elements (Mn, Cr, V, U, and Mo) show enrichments in the study sections.The stratigraphic position of the NRB is discussed in Supplementary Information.Blue dots represent raw data, and red lines show moving average on three samples.

Figure 2 .
Figure 2. U EF vs. Mo EF diagram for samples in the study sections.Base figure modified from Algeo and Tribovillard 38 .

Figure 4 .
Figure 4. Stratigraphic profiles of K EF , Rb EF , and CIA in the Pignola-Abriola section.Enrichment factors (EF) were calculated relative to UCC 60 .K EF and Rb EF decrease with increasing CIA values across the NRB.